Aluminum can activate grapevine defense through actin remodeling

Abstract

In the current study, we used a grapevine cell line in which actin filaments are labeled by GFP to show that aluminum causes actin remodeling through activation of NADPH oxidase in the plasma membrane, followed by activation of phytoalexin synthesis genes. Elimination of actin filaments by latrunculin B disrupts gene activation and inhibition of MAPK signaling by the inhibitor PD98059. Interestingly, aluminum also induces the transcription of ISOCHORISMATE SYNTHASE, a key enzyme for the synthesis of salicylic acid, as well as PR1, a gene that is known to be responsive to salicylic acid. However, while salicylic acid responses are usually a hallmark of the hypersensitive response, aluminum-triggered defense is not accompanied by cell death. Both actin remodeling and gene activation in response to aluminum can be suppressed by the natural auxin indole acetic acid, suggesting that the actin response is not caused by nonspecific signaling. Further evidence for the specificity of the aluminum-triggered activation of phytoalexin synthesis genes comes from experiments in which plant peptide elicitors induce significant cellular mortality but do not evoke induction of these transcription. The response in grapevine cells can be recapitulated in grapevine leaf discs from two genotypes contrasting in stilbene inducibility. Here, aluminum can induce accumulation of the central grapevine phytoalexin, the stilbene aglycone trans-resveratrol; this is preceded by a rapid induction of transcription for RESVERATROL SYNTHASE and the regulating transcription factor MYB14. The amplitude of this induction reflects the general stilbene inducibility of these genotypes, indicating that the aluminum effect is not caused by nonspecific toxicity but by activation of specific signaling pathways. The findings are discussed in relation to a model in which actin filaments activate a specific branch of defense signaling, acting in concert with calcium-dependent PAMP-triggered immunity. This pathway links the apoplastic oxidative burst through MAPK signaling with the activation of defense-related transcription.

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